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b"ç'aB r: The UniversitY of Adelaide Faculty of Agricultural and Natural Resource Sciences "The mode of action of Bacillus thuringiensis (Berliner) against the sheep lous e, Bovicolø ovis (Schrank)." by CATITERINE ALEXANDRA HILL Department of Crop Protection WAITE CAMPUS Glen Osmond, South Australia Thesis submitted in partial fulfilment of the requirements for the degree of Doctor of Philosophy. January, 1998. Frontispiece. Adult sheep biting lice, Bovicola ovis (Schrank) in the sheep fleece. SUMMARY Bacillus thuringiensrs, (Bt) produces a heterogeneous range of insecticidal toxins, the most notable being the ð-endotoxin crystal proteins effective against lepidopteran, dipteran and coleopteran larvae. Dulmage (1981) reported that certain strains of Bt produced an uncharacterised "louse factor" effective against phthirapteran species. Bt strain WB3S16, isolated from sheep fleece at the University of Adelaide, Waite Campus, causes very high mortality when ingested by the sheep biting louse B. ovis. This strain is currently being developed as a microbial insecticide for control of B. ovis. The objective of this study was to determine the nature and mode of action of the Bt strain \ryB3sl6 louse toxin effective against B. ovis. Bt fed B. ovis exhibit midgut disruption and histopathological effects which are similar to those of the ð-endotoxin crystal proteins in susceptible lepidopteran and coleopteran larvae (Hill and Pinnock, 1997). Investigations were made in this study to determine whether the Bt strain WB3S16 louse toxin is related or identical to the ð-endotoxin crystal proteins produced by this bacterium. A louse toxic factor was found in association with the Bt strain WB3S16 membranes and the culture supernatant following growth of the bacterium. The ð-endotoxin crystals were not toxic to B. ovis possibly because lice lack a midgut environment (Hill, 1992) essential for dissolution and activation of the â-endotoxin crystal into toxic peptides. However, WB3S16 â-endotoxin crystal proteins generated by in vitro dissolution of the crystal were highly toxic to B. ovis and caused a general paralysis, followed by death of the insect. Bt spores were not toxic per se to B. ovis, but caused septicaemia after they germinated in the gut of the insect. The toxicity of strain WB3S16 preparations was significantly reduced by treatment with proteases, suggesting that the WB3S16 louse toxin is proteinaceous. The louse toxin was produced from the vegetative cell stage through to sporulation. WB3S16 preparations became progressively more toxic to B. ovis as the culture matured and the toxicity of the Bt preparation correlated directly with an increase in the amount of crystal protein in the preparation. Strain WB3S16 produced 140kDa CrylA and 70kDa CryZA crystal proteins both of which were highly toxic to B. ovis and the CrylA was significantly more toxic to B. ovis than the Cry2A. Immunogold studies demonstrated specific binding of CrylA and Cry2A proteins to the midgut membrane of B. ovis. This result, together with the observed histopathological I effects, suggests that these proteins may bind to and form pores in B. ovis midgut cell membranes. The primary and secondary stmctures of the CrylA and Cry2A proteins deduced from sequences of cloned WB3S16 cryIA and cry2A genes were similar to those of other CrylA and Cry2A proteins. The novel host range of these proteins could not be attributed to major amino acid substitutions. The WB3S16 CrylA protein was highly susceptible to proteolytic degradation and degraded to a 70kDa protein over time. This characteristic may be a key to the lousicdal toxicity of strain WB3SI6. A 70kDa protein, immunologically related to the crystal proteins of strain V/B3S16 was found in association with the louse toxic membrane and supernatant fractions and was produced by louse toxic, crystal- Bt mutant strains generated by heat curing strain WB3S16 of plasmids bearing cry genes. The louse toxic strain WB3SI6 and crystal- mutant strains appeared to be producing a solubilised 70kDa crystal protein which for reasons unknown, was not incorporated into a crystal at time of formation. This protein which may be a Cry2A, a degraded form of the CrylA or a combination of both, was associated with the bacterial membranes and may be released to the supernatant when the cell lyses. Although lice do not dissolve and activate the crystal to toxic peptides, this solubilised or loosely adsorbed protein may act as a toxin against B. ovis following ingestion of the Bt preparation, by causing colloid osmolysis of midgut cells. This is the first study to report Bt crystal protein toxicity to a phthirapteran species. Although Bt strain WB3S16 may produce other unidentified toxins effective against B. ovis, these results summarised above have provided strong evidence that the ð-endotoxin crystal proteins of strain WB3S16 significantly contribute to the lousicidal toxicity of this strain. ll DECLARATION This work contains no material which has been accepted for the award of any other degree or diploma in any University or other tertiary institution and, to the best of my knowledge and belief, contains no material previously published or written by another person, except where due reference has been made in the text. I give consent to this copy of the thesis, when deposited in the University Library, being available for loan and photocopying. Catherine A. Hill lll ACKNOWLEDGMENTS I wish to thank my supervisors, Professors Dudley Pinnock, Otto Schmidt and Paul Manning for their input and continued guidance throughout this period of my scientific training. I am grateful to Professor Rick Roush and Dr Marianne Hellers who in conjunction with Professor Manning, supervised the cloning and sequencing studies. I would also like to thank the following people who provided assistance with various aspects of this project: Dr Chris Preston and Stephen Hole for HPLC analysis; Dr Ian Dundas for iso-electric focusing gels; Dr Marilyn Henderson for electron microscopy studies; and Juan Juttner for help with the southern blot analysis. To the former members of the Insect Pathology Laboratory and current members of the Department of Crop Protection, my thanks for fostering an environment which was conducive not only to study, but also to having fun. I express my appreciation to many close friends, in particular, Mandy Pace, Markus Beck and Leonie Simmons, who have helped me to maintain my sanity over the last four years. Finally, my gratitude to my family and to Matt McCallum, for their support and encouragement throughout my studies. 1V LIST OF ABBREVIATIONS ADP Adenosine diphosphate Ap Ampicillin AP Alkaline phosphatase ATP Adenosine triphosphate BBMV Brush border membrane vesicles ß-ME ß-mercaptoethanol BHIGYE Brain heart infu sion/glycine/yeast extract BLAST Basic local alignment search tool bp Base pair BSA Bovine serum albumin Bsp Bacillus sphaericus Bt B ac illus thur in g iens i s CP Crystal protein cps Counts per second Cry ð-endotoxin crystal protein cry â-endotoxin crystal protein gene crystal- Acrystalliferous Bt mutant strain cyt Cytolytic ð-endotoxin crystal protein cyt Cytolytic ð-endotoxin crystal protein gene ddH2O Distilled water doz Dissolved oxygen DNA Deoxyribonucleic acid dNTP adenine/cytosine/guanine/thymine nucleoside triphosphate DTT Dithiothreitol EDTA Disodium ethylenediaminetetraacetate ELISA Enzyme linked immuno-sorbent assay EMBL European Molecular Biology Laboratory EMP Embden-Meyerhoff-Parnas pathw ay FITC Fluoroscene iso-thio-cyanate GYS Glycine/yeast/salts medium HEPES N-[2-hydroxyethyl] piperazine-N' HPLC High perfonnance liquid chromatography HSB IIEPES salt buffer ICP Insecticidal crystal Protein IgG Gamma immunoglobulin IPTG Isopropylthio-ß-o- galactoside v kb Kilo base kDa Kilo dalton KSCN Potassium isothiocyanate LA Luria-Bertani agar LB Luria-Bertani medium LCso Lethal concentration value determined by probit analysis LV Lecitho-vitellin MDa Mega dalton MLP Modified lowry protein determination MOPS 3- [N -morpholino]propanesulphonic acid) buffer MW Molecular weight NA Nutrient agar NB Nutrient Broth NCBI National Centre for Biotechnology o/N Over night ORF Open reading frame PBS Phosphate buffered saline PC-PLC Phosphatidylcholine degrading phospholipase C enzyme PI-PLC Phosphatidylinositol-hydrolysing phospholipase C enzyme PCR Polymerase chain reaction PEGseso Polyethylene glycolssoo PIPES Piperazine-N, N'-bis[2-ethanesulphonic acid] PVP Polyvinyl-pynolidone 360 RAM Rabbit anti-mouse antibody RH Relative humidity RO Reverse osmosis purified water RNA Ribonucleic acid RNase Ribonuclease RT Room temperature sH2O Sterile water (autoclaved at I2I"C and lba¡ pressure for 20min) SDS Sodium dodecyl sulphate SDS-PAGE SDS polyacrylamide gel electrophoresis SSC Sodium citrate buffer subsp. subspecies TAE Tris-acetate electrophoresis buffer TBE Tris-borate electrophoresis buffer TBS Tris buffered saline TCA Tricarboxylic acid cycle TE TrisÆDTA buffer TEMED N, N, N', N'-Trametþlethylenediamine TES TrisÆDTA/Sucrose buffer vi Tris Tris(hydroxymethyl)aminomethane hydrochloride TTBS Tween-Tris buffered saline Tween-20 polyoxyethylene (20) sorbitan mono-oleate Type Itr RO water Triple distilled Millipore water. vlv volume/volume w/v weighUvolume X-gal 5 -Bromo-4-chloro-3 -indolyl-ß-o- galactoside vll TABLE OF CONTENTS I Summary Decla¡ation 111 Acknowledgments iv List of Abbreviations v 1. Literature Review I l.l Bovicola ovis 1 l. 2 Bacillus thuringiensis 1 n 1.2. I History of Bt and its Commercial Production 1.2.2 Cell Morphology and Historical Classification 3 4 1. 3 ð-endotoxin Crystal Proteins 1. 3. 1 Genetic Aspects of crystal Protein Production in Bt 4 I.3.2 Crystal Protein Nomenclature 4 L.3.3 Composition of ð-endotoxin Crystals 5 I.3.4 Cryl and Cry2 Crystal Proteins 5 1. 3. 5 Structure of Crystal Proteins 6 1. 3. 6 Mode of Action of Crystal Proteins 7 1.3.7 Histopathological Effects of Crystal Proteins 8 1. 3. 8 Sequencing and Expression of cry Genes 9 1.3.9 CYt Toxins 10 l. 3. 10 Bt subsP. kurstaki Strains 10 1. 3. l1 Bt Devetopment and Formation of the ð-endotoxin Crystal 11 1.3.
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